Mu llerian Anomalies. Introduction

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1 CLINICAL OBSTETRICS AND GYNECOLOGY Volume 51, Number 1, r 2008, Lippincott Williams & Wilkins Mu llerian Anomalies LEE P. SHULMAN, MD The Anna Ross Lapham Professor in Obstetrics and Gynecology, Department of Obstetrics and Gynecology, Feinberg School of Medicine, Northwestern University, NMH/Prentice Women s Hospital, Chicago, Illinois Abstract: Mu llerian anomalies are a relatively uncommon occurrence with implications for adolescents and adults as they may result in specific gynecologic, fertility, and obstetrical issues. The exact incidence of Mu llerian anomalies is difficult to ascertain. However, clinicians should be suspicious for Mu llerian anomalies in cases of primary amenorrhea, pelvic pain, repetitive pregnancy loss, and certain adverse obstetrical outcomes. While for many women a good reproductive outcome can be achieved, counseling, and in particular psychologic counseling, may be needed for some women, especially those with lesions that preclude childbearing and affect normal sexual function. Key words: Mu llerian, anomalies, didelphys, recurrent miscarriage Correspondence: Lee P. Shulman, MD, 250 East Superior Street, Room , Chicago, IL lshulman@nmh.org Introduction The normal development of the female reproductive tract involves a complex integrative series of events involving genetic, hormonal, and epigenetic factors leading to the normal differentiation and development of the Mu llerian, or paramesonephric, ducts, Wolffian, or mesonephric, ducts, and urogenital sinus. Accordingly, any one of numerous alterations in this process can lead to abnormalities of the uterus, cervix, fallopian tubes, or vagina. Depending on the specific abnormality, affected women may experience gynecologic, fertility, or obstetrical problems. Nonetheless, the true incidence of Mu llerian anomalies is difficult, if not impossible, to determine because of the considerable variation in presentation. Some anomalies may lead to clinical problems in childhood, whereas other anomalies may only be detected serendipitously at the time of a clinical evaluation or surgical procedure for another medical condition. In addition, although most cases of Mu llerian anomalies occur in an isolated fashion, some anomalies are components of congenital syndromes. Most women with Mu llerian anomalies demonstrate no problems with menstruation or conception. However, women with Mu llerian anomalies do present with higher rates of spontaneous abortion, premature delivery, abnormal fetal position, and dystocia. 1 Accordingly, an overview of Mu llerian anomalies is important for a more complete understanding of female sexual development and of those clinical gynecologic and obstetrical issues that do require intervention during the pediatric, adolescent, and reproductive years. CLINICAL OBSTETRICS AND GYNECOLOGY / VOLUME 51 / NUMBER 2 / JUNE

2 Embryology Male (Wolffian or mesonephric) and female (Mu llerian or paramesonephric) duct systems are indistinguishable in fetuses at or before 6 weeks of development. The absence of a Y chromosome, in most of the cases, results in the development of ovaries. Without testosterone, the Wolffian ducts regress and permit the development of the Mu llerian ducts. Conversely, regression of the Mu llerian ducts requires the presence of a protein (MIS or Mu llerian-inhibiting substance) that is secreted by the testis. In the absence of MIS, the Mu llerian ducts develop on the lateral surface of the mesonephric ducts, with the superior portions going on to form the fallopian tubes whereas the posterior portions fuse into a Y-shaped structure that develops into the uterus, cervix, and superior portion of the vagina. 2 Indeed, alterations of this process at any stage can lead to Mu llerian anomalies that can impact normal female development and sexual function. Epidemiology Because of the wide variation of clinical presentation of Mu llerian anomalies, assessment of prevalence is challenging insofar as some anomalies are detected at an early age whereas others are only detected as a result of evaluation or treatment for nonrelated medical conditions. Accordingly, the reported prevalence has ranged from 0.16% to 10%. 1 However, the actual ascertainment of the anomaly is a critical determinant of the reported frequency of the anomaly. For example, Stampe Sorensen 3 reported a prevalence of 8% to 10% among infertile women undergoing hysterosalpingography (HSG) whereas Byrne and colleagues 4 reported an incidence of 0.4% in women undergoing ultrasound examinations for nonobstetrical indications. As expected, evaluation of an unselected population usually results in a considerably lower Mu llerian Anomalies 215 frequency of Mu llerian anomalies than the evaluation of a specific cohort identified as result of a condition (eg, infertility) that has been associated with Mu llerian anomalies. Classification and Clinical Effects Most clinicians use the classification system devised by Buttram and Gibbons in 1979, 5 as this scheme categorized the various anomalies based on clinical presentation. Although some of the conditions within each class may originate from different embryologic embarrassments, this system does provide a useful clinical tool for determining intervention and prognosis (Fig. 1). Class I: segmental agenesis and various degrees of uterovaginal hypoplasia. This group includes Mu llerian agenesis and vaginal agenesis. Class II: unicornuate uterus. Class III: uterus didelphys. Class IV: bicornuate uterus and varying degrees of incomplete fusion of the superior segments of the uterovaginal canal. Class V: varying degrees of septate uterus. Class VI: varying degrees of arcuate uterus. Class VII: sequela of DES exposure. The most common Mu llerian anomaly is the septate uterus (Class V), comprising over 50% of all reported Mu llerian anomalies. This condition is the result of partial or incomplete failure of the resorption of the uterovaginal septum after the fusion of the paramesonephric ducts. Among those Müllerian anomalies that permit pregnancy, Class V anomalies are associated with a marked reduction in the ability to maintain a pregnancy. Troiano and McCarthy 1 report that pooled data show the prevalence of septa in women with recurrent spontaneous pregnancy losses ranges from 26% to 94%. In addition, septate uteri are also associated with adverse obstetrical outcomes, with preterm birth rates in women

3 216 Shulman FIGURE 1. Uterine fusion anomalies: I, Septate uterus; II, bicornuate uterus; III, unicornuate uterus; IV, uterus didelphys; V, normal uterus; VI, arcuate uterus. with septate uteri ranging from 9% to 30% and a commensurate reduction in fetal survivability. The differentiation between the septate uterus and the Class IV anomalies (bicornuate uterus) is based on the external appearance of the uterus. Although these 2 classes of anomalies result from different embryologic processes the bicornuate uterus, the second most common Mu llerian anomaly making up approximately 10% of all such abnormalities, is the result of incomplete fusion of the uterovaginal horns. This differentiation is critical as the interventions for these 2 classes are widely different. Septate uterus is usually amenable to hysteroscopic resection whereas the bicornuate uterus usually does not require intervention except in those who have experienced multiple late-term pregnancy losses. In those cases, the Strassman metroplasty is still used to unify the 2 cavities and restore the contour of the external uterus. Uterus didelphys (Class III) accounts for approximately 5% of Mu llerian anomalies and is the result of nearly complete failure of the fusion of the paramesonephric ducts. Indeed, this anomaly represents a more complete embarrassment in the embryologic process that unites the 2 paramesonephric ducts. In such cases, each duct develops into an almost separate uterine hemicavity either sharing a cervix or, in some cases, with its own cervix. Without obstruction, uterus didelphys is asymptomatic. However, many cases can be associated with obstruction by vaginal septa and thus present with progressive menarchal dysmenorrhea that can lead to endometriosis and pelvic adhesive disease. Unicornuate uterus results from the failure of 1 of the 2 paramesonephric ducts to develop. Surprisingly, the Class II anomalies account for almost 1/5 of all Mu llerian anomalies. Unicornuate uterus may present as a totally isolated anomaly, but usually (approximately 2/3 of all such cases) presents in concert with a rudimentary horn. Approximately half of such rudimentary horns have some endometrial tissues whereas half do not. Interestingly, most unicornuate uteri are present on the right side, a phenomenon that has yet to be explained. This anomaly is associated with an increased risk for spontaneous loss and

4 Mu llerian Anomalies 217 preterm labor, apparently associated with the reduction in available uterine muscle mass and deformation of the available endometrial cavity. Our group 6 has recently reported on the successful use of multifetal pregnancy reduction for those women carrying more than 1 fetus in a unicornuate uterus. In addition, in those women with a noncommunicating rudimentary horn with endometrial tissue, initial presentation may occur at menarche with progressive dysmenorrhea. The Class I anomalies represent the most severe interruption of gynecologic function and account for 8% to 10% of Mu llerian anomalies. However, both forms of Class I Mu llerian anomalies present with no obvious phenotypic abnormalities at birth and only are detected at menarche. Mu llerian agenesis, also known as Mayer-Rokitansky-Kuster- Hauser syndrome, presents with primary amenorrhea with normal secondary sexual development. Vaginal agenesis also presents with normal secondary sexual development but with increasing dysmenorrhea as this condition usually does not preclude the development of more superior positioned, and thus endometrial-containing tissues, that have no communication with the vagina and thus lead to the progressive dysmenorrhea associated with other obstructive conditions. Mu llerian aplasia may also be a component of syndromes involving nonpelvic organs, the most common being Mu llerian renal cervical spine. As such conditions preclude reproduction, it is difficult to assess the exact genetic or epigenetic mechanisms responsible for this condition. Nonetheless, this grouping of Mu llerian aplasia, renal anomalies such as horseshoe kidney, and cervical spine abnormalities including fused vertebra, rudimentary vertebral bodies, and Klippel-Feil anomalad (cervical vertebral fusion, reduced range of motion, low hairline) may occur in almost 10% of women with Mu llerian aplasia. Although most individuals with Mu llerian anomalies do not have chromosome abnormalities, a few females with Mu llerian anomalies have been found to have chromosome abnormalities including mosaic sex complements (45,X/46,XX) and autosomal deletions. In addition, our group 7 has reported on an individual with Mu llerian renal cervical spine and other associated nongynecologic structural abnormalities, providing evidence of the potential for genetic, epigenetic, and environmental factors in the abnormal development of the female reproductive tract. Symptoms are dependent on the presence or absence of functional endometrium. With no symptoms of progressive dysmenorrhea, intervention can be delayed until the commencement of sexual activity. Although specific symptoms may lead to specific interventions, a nonsurgical approach known as Frank s vaginal dilation is commonly used and is considered to be the initial treatment of choice. This approach uses serial dilation of the rudimentary vagina with dilators. The most commonly used surgical approach is the Abbe-McIndoe approach and involves the construction of a neovagina by careful dissection of the tissue between the urethral opening and the posterior fourchette. In case of vaginal agenesis, removal of the endometrial-containing tissue is now readily accomplished by a laparoscopic approach. Because of the profound sexual and fertility implications of these Class I anomalies, referral for more detailed and extensive counseling should be strongly considered. Indeed, referral to a psychologist or psychiatrist is warranted for those girls or women and their families when finding out that they are unable to conceive and will need some intervention for normal sexual function. At our center, such a referral is a routine part of the diagnostic and therapeutic process for all who are found to have such Mu llerian anomalies.

5 218 Shulman FIGURE 2. Transverse vaginal septa. X points to most common site of occurrence. In addition to the obstructive conditions described above, vaginal septa can present with partial or complete obstruction. Such septa are the result of late fusion defects: vertical fusion defects lead to transverse septa whereas lateral fusion defects lead to longitudinal septa (Figs. 2, 3). Thetransverseseptumismorelikelyto lead to symptoms at the time of menarche, as such obstructions are more likely to block the flow of menstruum and lead to the symptoms associated with other obstructive conditions. Longitudinal septa are less likely to lead to obstruction, and may not be found until the initiation of sexual activity or pelvic examinations. Obstructive septa can be excised by vaginal resection of the septum; nonobstructive septa may need no intervention if such tissue does not complicate menstruation, sexual activity, pelvic examination, or obstetrical processes. The Class VI anomalies represent the anomalies that are least likely to result in FIGURE 3. Longitudinal vaginal septum.

6 Mu llerian Anomalies 219 adverse developmental, fertility or obstetrical outcomes. The arcuate uterus is characterized by a fundal indentation of the endometrium resulting from a minimally incomplete resorption of the uterovaginal septum. Indeed, some believe that the arcuate uterus represent a normal variant rather than an actual anomaly. Although there are data that support and refute an adverse clinical impact of the arcuate uterus, the only indication to pursue intervention would be recurrent pregnancy loss and the approach would be a hysteroscopic resection of prominent fundal tissue detected by HSG or some other imaging technique. Those Mu llerian anomalies (Class VII) attributed to in-utero DES exposure are decreasing in frequency with the cessation of the use of DES by pregnant women by the beginning of the 1980s. A full review of the diagnosis, implications and management of DES progeny is beyond the scope of this chapter. Diagnosis Diagnosis of Mu llerian anomalies is primarily based on the clinical presentation, including the temporal nature of the initial presentation, the nature of the presenting symptoms, and the particular portion(s) of the pelvis that may be affected by the Mu llerian anomaly. Accordingly, a detailed history, including family history, and a physical examination including assessment of the pelvic structures is a necessary first step in assessing the potential causes of the presenting symptoms and suggesting possible interventions. A very small percentage of females with Mu llerian anomalies are found to have a Mendelian disorder such as the autosomal dominant hand-foot-uterus syndrome, the autosomal recessive Fraser syndrome and the X-linked uterine-hernia syndrome. 2 However, such individuals will present with the profound clinical findings of the Mendelian disorder and be found to have Mu llerian anomalies as part of the secondary evaluation. Nonetheless, women s healthcare providers may be called upon to consult in the evaluation of certain gynecologic conditions in such affected girls and women; consideration of Mu llerian anomalies in such cases is strongly warranted and the appropriate cytogenetic and imaging evaluation should be provided as in females who do not present with concomitant Mendelian disorders. In most cases of Mu llerian anomalies, affected individuals present with normal secondary sexual development. Although some presentations are suggestive of a potential chromosomal abnormality (almost always involving the sex chromosomes), most Mu llerian anomalies are not associated with autosomal or sex chromosome abnormalities. Nonetheless, some clinical presentations involving possible abnormalities in sexual development, fertility, and maintenance of pregnancy may involve chromosome abnormalities and consideration of such testing is warranted in many, but not in all, such cases. The use of other laboratory tests such as serum sex steroid levels and other assays are usually not indicated as a general or universal assessment, except in the presence of specific clinical symptoms. As such, clinicians should avoid the routine use of laboratory tests that are unlikely to provide any useful information in the evaluation of affected girls or women. Primary amenorrhea is perhaps one of the most important and noticeable initial presenting symptoms, strongly suggestive of an obstructive anomaly. More so than other clinical signs, primary amenorrhea can be representative of a variety of etiologies, including cytogenetic abnormalities, Mendelian disorders, and isolated Mu llerian anomalies. The most important initial assay to obtain in such individuals is a karyotypic analysis. Finding a 46,XY complement should lead the clinician to consider one

7 220 Shulman of the conditions affecting normal testosterone function, including abnormalities in receptor function or 5-a reductase abnormalities. In these cases, there is no concern regarding Mu llerian anomalies as the testes still produce MIS and there are usually no normal Mu llerian structures. A concern for such females, as well as those found to have mosaic complements with Y-bearing chromosome lines, is the potential for the development of gonadal malignancies. The timing of gonadal extirpation, which is needed to prevent the development of gonadal malignancy, will vary depending on the particular abnormality. In cases of 46 XX, an assessment of pelvic organs is critical in determining the cause of the amenorrhea. Finding a blindending and shortened vagina (with no visible cervix) should lead the clinician to consider a Class I anomaly, which can be evaluated by ultrasound or magnetic resonance imaging (MRI). 1,8 12 However, some cases may require intra-abdominal assessment, and in such cases, laparoscopy can provide diagnostic and therapeutic interventions in selected cases. 13 As most affected females with primary amenorrhea go through normal secondary sexual development save for the absence of menstruation, the diagnosis of Mu llerian anomalies leading to primary amenorrhea or any other clinical presentation is frequently accomplished during adolescence. 14 The presence of pelvic pain, especially progressive in nature, at a time usually associated with the onset of menses, provides important information to the clinician. Such cases are clearly associated with functioning endometrium, and the assessment again depends on the findings of the physical examination (eg, presence or absence of a cervix). In such cases, ultrasound and MRI provide important critical information. Dyspareunia is also associated with vaginal septa; however, most such cases are not associated with primary amenorrhea and are unlikely to represent a totally obstructive lesion such as the transverse septum that completely obstructs the outflow of menstruum. Indeed, like other cases characterized by obstructive anomalies with intact endometrial tissue, females with such lesions are likely to present with primary amenorrhea and progressive pelvic pain rather than dyspareunia at a later time in their lives. Most women with Mu llerian anomalies do not present with primary amenorrhea, and as such, assessment of the reasons for presentation weigh heavily in determining the appropriate assessment. In women presenting with repetitive pregnancy loss, an HSG has been the conventional imaging technology used for determining the presence of Mu llerian anomalies. In women with progressive pain, or dyspareunia, or some chronic pelvic pain, a combination of imaging technologies (including HSG, MRI, and ultrasound) and laparoscopy may be needed to evaluate and possibly treat such conditions. For some conditions such as intrauterine septa, hysteroscopy may be needed to confirm the diagnosis and provide the necessary approach for resection and treatment. 15 Pain and primary amenorrhea are important clinical signs associated with Mu llerian anomalies. However, most women with Mu llerian anomalies will experience neither amenorrhea nor pain as a result of having Mu llerian anomaly. Infertility, repetitive pregnancy loss, repetitive poor obstetrical outcomes (occurrences of preterm labor or second/ third trimester loss), chronic pelvic pain, and dyspareunia may also indicate the presence of Mu llerian anomalies. Depending on the presentation, imaging technologies such as HSG, ultrasound (2D and 3D) and MRI, laparoscopy and hysteroscopy may be needed to properly evaluate the pelvic structures and determine the presence of Mu llerian anomaly.

8 Mu llerian Anomalies 221 Treatment for Mu llerian anomalies is highly specific to the anomaly detected and the desired clinical outcome. Depending on the specific anomaly, hysteroscopy, laparoscopy and, in uncommon or somewhat complex clinical presentations, laparotomy may be needed to relieve the obstruction, reform the affected organ and provide for a salutary clinical outcome. For women who present with infertility or poor obstetrical outcomes, surgery may be needed to relieve the malformation leading to the adverse outcomes. However, management of these anomalies remains controversial with few rigorous scientific trials to provide robust information for clinicians and women seeking improved reproductive outcomes. In general, surgical intervention is usually indicated for women with Mu llerian anomalies who present with obstructive anomalies, pelvic pain (especially when it s progressive in nature), endometriosis, repetitive pregnancy loss, and repetitive adverse obstetrical outcomes. 16 Conclusions Mu llerian anomalies are a relatively uncommon occurrence with implications for adolescents and adults with specific gynecologic, fertility, and obstetrical issues. Certain anomalies are more likely to present in the adolescent years, whereas others are more likely to present during the reproductive years. Clinicians should be suspicious for Mu llerian anomalies in cases of primary amenorrhea, pelvic pain, repetitive pregnancy loss, and certain adverse obstetrical outcomes. Imaging technologies, laparoscopy, and hysteroscopy are the major diagnostic tools; however, critical information is always obtained by a thorough history and physical. Interventions are usually determined by the actual anomaly, the clinical presentation, and the desired clinical outcome and usually involve laparoscopy and hysteroscopy, although laparotomy may be needed in a small number of select cases. Although good clinical outcomes can be achieved, many such anomalies, even when treated in optimal fashion, may not provide the desired fertility obstetrical outcomes. Counseling, and in particular psychologic counseling, may be needed for some women, especially those with Class I lesions that invariably preclude childbearing and affect normal sexual function. References 1. Troiano RN, McCarthy SM. Mu llerian duct anomalies: imaging and clinical issues. Radiology. 2004;233: Shulman LP, Elias S. Developmental abnormalities of the female reproductive tract: pathogenesis and nosology. Adolesc Pediatr Gynecol. 1988;1: Stampe Sorensen S. Estimated prevalence of mullerian anomalies. Acta Obstet Gynecol Scand. 1988;67: Byrne J, Nussbaum-Black A, Taylor WS, et al. Prevalence of Mullerian duct anomalies detected at ultrasound. Am J Med Genet. 2000;94: Buttram VC Jr, Gibbons WE. Mullerian anomalies: a proposed classification. Fertil Steril. 1979;32: Shulman LP, Ginsberg NA, Dungan JS, et al. Fetal reduction I cases of maternal uterine anomalies. Presented at the Annual Meeting of the Central Association of Obstetricians and Gynecologists, Chicago, IL, Gilliam M, Shulman LP, Scommegna A. Tetrology of fallot, imperforate anus, Mu llerian, renal and cervical spine (MURCS) anomalies in a 15-year-old girl. J Pediatr Adolesc Gynecol. 2002;15: Lindenman E, Shepard MK, Pescovitz OH. Mu llerian agenesis: an update. Obstet Gynecol. 1997;90: Folch M, Pigem I, Konje JC. Mu llerian agenesis: etiology, diagnosis and management. Obstet Gynecol Surv. 2000;55: Lin PC. Reproductive outcomes in women with uterine anomalies. J Womens Health. 2004;13:33 41.

9 222 Shulman 11. Mueller GC, Hussain HK, Smith YR, et al. Mu llerian duct anomalies: comparison of MRI diagnosis and clinical diagnosis. AJR. 2007;189: Wu M-H, Hsu C-C, Huang K-H. Detection of congenital Mu llerian duct anomalies using three-dimensional ultrasound. J Clin Ultrasound. 1997;25: Strawbridge LC, Crouch NS, Cutner AS, et al. Obstructive Mu llerian anomalies and modern laparoscopic management. J Pediatr Adolesc Gynecol. 2007;20: Spence JE. Vaginal and uterine anomalies in the pediatric and adolescent patient. J Pediatr Adolesc Gynecol. 1998; 11: Di Spiezio SA, Guida M, Bettocchi S, et al. Role of hysteroscopy in evaluating chronic pelvic pain. Fertil Steril. Epub Sept 17, Rackow BW, Arici A. Reproductive performance of women with Mu llerian anomalies. Curr Opin Obstet Gynecol. 2007;19:

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